Title : Variation in a Poaceae-conserved fatty acid metabolic gene cluster controls rice yield by regulating male fertility.
Abstract:
Unlike in bacteria, where genes associated with the same metabolic pathway are often clustered to form operons, in eukaryotes, most of the non-homologous genes involved in the same metabolic pathway are scattered throughout the genome and only some non-homologous genes in the metabolic pathways of fungi and plants function by aggregating to form gene clusters. A Metabolic Gene Cluster (MGC) is a cluster of at least three genes encoding different enzymes involved in the same metabolic pathway that controls the accumulation of metabolites. Most of the reported MGCs are for secondary metabolites, and fatty acid MGCs have not yet been discovered, nor have primary MGCs in planta. Here, combining with metabolic and phenotypic genome-wide association studies, we identify a major locus containing a six-gene fatty acid metabolic gene cluster on chromosome 3 (FGC3) that controls the cutin monomer Hydroxy Monoacyl Glycerols (HMGs) contents and rice yield, possibly through variation in the transcription of FGC3 members. We show that HMGs are sequentially synthesized in the endoplasmic reticulum by OsFAR2, OsKCS11, OsGPAT6, OsCYP704B2 and subsequently transported to the apoplast by OsABCG22 and OsLTPL82. Mutation of FGC3 members reduces HMGs, leading to defective male reproductive development and a significant decrease in yield. OsMADS6 and OsMADS17 directly regulate FGC3 and thus influence male reproduction and yield. FGC3 is conserved in Poaceae and likely formed prior to the divergence of pharus latifolius. The eukaryotic fatty acid and plant primary metabolic gene cluster we identified show a significant impact on the origin and evolution of Poaceae and has potential for application in hybrid crop breeding. The present study identifies HMG components in rice anther cuticles, a class of metabolites previously described in stephanotis floribunda, prunus laurocerasus and citrus aurantium. These findings help elucidate cutin monomer metabolism, improve the network of HMG synthesis, transport and regulation, and lay a foundation for further study of male reproductive development. In particular, it was reported that the MADS family gene regulates male reproductive development in rice through cutin monomer metabolism. The anther surface and pollen exine are covered with lipid layers that consist of fatty acid derivative hydroxy fatty acids and HMGs, which are critical for male reproductive development, protecting the male gametophytes from dehydration and facilitating subsequent pollen-stigma communication and adhesion, and thus any disruption of these layers often leads to microspore abortion and male sterility. By identifying the functions of genes in FGC3 and further optimizing the components of this gene cluster, related genes can be engineered to help produce crops resistant to low humidity environmental stress and expand crop planting areas.
